Light, Not Age, Underlies the Maladaptation of Maize and Miscanthus Photosynthesis to Self-Shading

Abstract

Zea mays and Miscanthus × giganteus use NADP-ME subtype C₄ photosynthesis and are important food and biomass crops, respectively. Both crops are grown in dense stands where shaded leaves can contribute a significant proportion of overall canopy productivity. This is because shaded leaves, despite intercepting little light, typically process light energy very efficiently for photosynthesis, when compared to light-saturated leaves at the top of the canopy. However, an apparently maladaptive loss in photosynthetic light-use efficiency as leaves become shaded has been shown to reduce productivity in these two species. It is unclear whether this is due to leaf aging or progressive shading from leaves forming above. This was resolved here by analysing photosynthesis in leaves of the same chronological age in the centre and exposed southern edge of field plots of these crops. Photosynthetic light-response curves were used to assess maximum quantum yield of photosynthesis; the key measure of photosynthetic capacity of a leaf in shade. Compared to the upper canopy, maximum quantum yield of photosynthesis of lower canopy leaves was significantly reduced in the plot centre; but increased slightly at the plot edge. This indicates loss of efficiency of shaded leaves is due not to aging, but to the altered light environment of the lower canopy, i.e., reduced light intensity and/or altered spectral composition. This work expands knowledge of the cause of this maladaptive shade response, which limits productivity of some of the world's most important crops.

Keywords: C4 photosynthesis; bioenergy; canopy; food security; leaf aging; photosynthetic light-use efficiency; quantum yield; shade acclimation.

FIGURE 1

Average response curves of A to PPFD in both canopy positions (upper, lower) of (A) Z. mays in plot centre and (B) plot edge; and (C) M. x giganteus in plot centre and (D) plot edge (n = 8–16). Symbols give the mean A ± s.e. at each level of PPFD. Lines give the non-rectangular hyperbolae fit to these measurements. In each panel, the inset shows the light-limited section of the response curve (PPFD from 40 to 140 μmol m^–2 s^–1), used to estimate maximum quantum yields by linear regression: the slope of this regression gives the trait ϕCO_{2 max, app}.

FIGURE 2

Mean ± s.e. for (A) ϕCO_{2 max,abs}, (B) A_sat, (C) F_v/F_m, (D) α, (E) 1/k, and (F) R_d for Z. mays and M. x giganteus for upper and lower canopy leaves in both plot positions (centre, edge) (n = 8–16). p-values are from ANOVA testing the fixed effects of species, plot position, canopy position, and all two-way interactions. Significant p-values (< 0.05) are in bold black. Marginally significant p-values (< 0.1) are in bold grey.

FIGURE 3

Average linear responses of A to J in (A) Z. mays in plot centre and (B) plot edge; and (C) M. x giganteus in plot centre and (D) plot edge (n = 8–16). Data is from light-limited measurements (PPFD from 40 to 140 μmol m^–2 s^–1). Symbols give the mean A ± s.e. and mean J ± s.e. at each level of PPFD. Lines give the best-fit linear regression; the slope of this regression gives the trait 1/k.